Skip to main content

Advertisement

SpringerLink
Log in

Nitric oxide regulates polarity of guinea pig distal colon pellet propagation and circular muscle motor response

  • Original Article—Alimentary Tract
  • Published:
Journal of Gastroenterology Aims and scope Submit manuscript

Abstract

Background

Peristaltic reflex does not fully explain the polarity of peristalsis. In the distal colon, we propose that the balance of circular muscle contraction proximal and distal to the pellet is a local reflex that predicts polarity of peristalsis.

Methods

Guinea pig distal colon segments were harvested, and fecal pellet transit was measured. Photographs of fecal pellet propagation were taken, colonic radius proximal and distal to the moving pellet was measured, and the ratio of radius proximal to pellet to radius distal to pellet was measured. Isometric transducers were attached 1 cm proximal and distal to a fixed intraluminal balloon, and circular muscle (CM) response to balloon distension was recorded. N G-Nitro-l-arginine methyl ester hydrochloride (L-NAME) was used to elicit an effect in experimental preparations and compared to controls.

Results

Fecal pellet transit was delayed after L-NAME treatment (163 ± 23.9 vs. 41.5 ± 1.9 s in control, n = 6, p < 0.001). Photo-analysis revealed a ratio of proximal/distal colonic radius in control colon to be 0.72 ± 0.02 (n = 17) and in L-NAME treated colon 1.0 ± 0.02 (n = 10, p < 0.01). The dominant CM response pattern was a large contraction proximal to the inflated balloon and a smaller contraction distal to the balloon. In the presence of L-NAME, distal contraction was larger than the proximal contraction in 66 % of the experiments.

Conclusions

Pellet propulsion in the guinea pig's distal colon depends on nitric oxide to provide appropriate balance of force between proximal and distal contraction, resulting in pellet propagation toward the anus. CM contracts both proximal and distal to the pellet, and the polarity of pellet progression depends on the balance of the two forces.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

ACh:

Acetylcholine

ATP:

Adenosine triphosphate

NO:

Nitric oxide

VIP:

Vasoactive intestinal peptide

CM:

Circular muscle

LM:

Longitudinal muscle

L-NAME:

N G-Nitro-l-arginine methyl ester hydrochloride

MI:

Motility index

KHB:

Krebs–Henseleit buffer

References

  1. Bayliss WM, Starling EH. The movements and innervation of the small intestine. J Physiol. 1899;24:99–143.

    CAS  PubMed Central  PubMed  Google Scholar 

  2. Costa M, Furness JB. The peristaltic reflex: an analysis of the nerve pathways and their pharmacology. Naunyn Schmiedebergs Arch Pharmacol. 1976;294:47–60.

    Article  CAS  PubMed  Google Scholar 

  3. Cannon WB. Peristalsis, segmentation, and the myenteric reflex. Am J Physiol. 1912;30:114–28.

    Google Scholar 

  4. Hirst GD, McKirdy HC. A nervous mechanism for descending inhibition in guinea-pig small intestine. J Physiol. 1974;238:129–43.

    CAS  PubMed Central  PubMed  Google Scholar 

  5. Smith TK, Bornstein JC, Furness JB. Interaction between reflexes evoked by distension and mucosal stimulation: electrophysiological studies of guinea-pig ileum. J Auton Nerv Syst. 1991;34:69–76.

    Article  CAS  PubMed  Google Scholar 

  6. Bornstein JC, Costa M, Grider JR. Enteric motor and interneuronal circuits controlling motility. Neurogastroenterol Motil. 2004;16(Suppl 1):34–8.

    Article  PubMed  Google Scholar 

  7. Grider JR, Makhlouf GM. Colonic peristaltic reflex: identification of vasoactive intestinal peptide as mediator of descending relaxation. Am J Physiol. 1986;251:G40–5.

    CAS  PubMed  Google Scholar 

  8. Smith TK, McCarron SL. Nitric oxide modulates cholinergic reflex pathways to the longitudinal and circular muscle in the isolated guinea-pig distal colon. J Physiol. 1998;512(Pt 3):893–906.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Smith TK, Robertson WJ. Synchronous movements of the longitudinal and circular muscle during peristalsis in the isolated guinea-pig distal colon. J Physiol. 1998;506(Pt 2):563–77.

    CAS  PubMed Central  PubMed  Google Scholar 

  10. Spencer NJ, Dickson EJ, Hennig GW, Smith TK. Sensory elements within the circular muscle are essential for mechanotransduction of ongoing peristaltic reflex activity in guinea-pig distal colon. J Physiol. 2006;576:519–31.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Spencer NJ, Hennig GW, Smith TK. Stretch-activated neuronal pathways to longitudinal and circular muscle in guinea pig distal colon. Am J Physiol Gastrointest Liver Physiol. 2003;284:G231–41.

    CAS  PubMed  Google Scholar 

  12. Spencer NJ, Smith TK. Simultaneous intracellular recordings from longitudinal and circular muscle during the peristaltic reflex in guinea-pig distal colon. J Physiol. 2001;533:787–99.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Spencer N, Walsh M, Smith TK. Does the guinea-pig ileum obey the ‘law of the intestine’? J Physiol. 1999;517(Pt 3):889–98.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Huizinga JD, Lammers WJ. Gut peristalsis is governed by a multitude of cooperating mechanisms. Am J Physiol Gastrointest Liver Physiol. 2009;296:G1–8.

    Article  CAS  PubMed  Google Scholar 

  15. Tonini M, Costa M, Brookes SJ, Humphreys CM. Dissociation of the ascending excitatory reflex from peristalsis in the guinea-pig small intestine. Neuroscience. 1996;73:287–97.

    Article  CAS  PubMed  Google Scholar 

  16. Bozler E. Reflex peristalsis of the intestine. Am J Physiol. 1949;157:338–42.

    CAS  PubMed  Google Scholar 

  17. Bozler E. Myenteric reflex. Am J Physiol. 1949;157:329–37.

    CAS  PubMed  Google Scholar 

  18. Ji SW, Park H, Chung JP, Lee SI, Lee YH. Effects of tegaserod on ileal peristalsis of guinea pig in vitro. J Pharmacol Sci. 2004;94:144–52.

    Article  CAS  PubMed  Google Scholar 

  19. Hirst GD, Holman ME, McKirdy HC. Two descending nerve pathways activated by distension of guinea-pig small intestine. J Physiol. 1975;244:113–27.

    CAS  PubMed Central  PubMed  Google Scholar 

  20. Mizuta Y, Takahashi T, Owyang C. Nitrergic regulation of colonic transit in rats. Am J Physiol. 1999;277:G275–9.

    CAS  PubMed  Google Scholar 

  21. Van Geldre LA, Lefebvre RA. Interaction of NO and VIP in gastrointestinal smooth muscle relaxation. Curr Pharmaceut Des. 2004;10:2483–97.

    Article  Google Scholar 

  22. Nicholas S, Spencer NJ. Peristalsis and fecal pellet propulsion do not require nicotinic, purinergic, 5-HT3, or NK3 receptors in isolated guinea pig distal colon. Am J Physiol Gastrointest Liver Physiol. 2010;298:G952–61.

    Article  CAS  PubMed  Google Scholar 

  23. Kerwin JF Jr, Heller M. The arginine-nitric oxide pathway: a target for new drugs. Med Res Rev. 1994;14:23–74.

    Article  CAS  PubMed  Google Scholar 

  24. Holzer P, Lippe IT, Tabrizi AL, Lenard L Jr, Bartho L. Dual excitatory and inhibitory effect of nitric oxide on peristalsis in the guinea pig intestine. J Pharmacol Exp Ther. 1997;280:154–61.

    CAS  PubMed  Google Scholar 

  25. Kono T, Chisato N, Ebisawa Y, Asama T, Sugawara M, Ayabe T, et al. Impaired nitric oxide production of the myenteric plexus in colitis detected by a new bioimaging system. J Surg Res. 2004;117:329–38.

    Article  CAS  PubMed  Google Scholar 

Download references

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Surgery, Medical College of Wisconsin and Clement J Zablocki VA Medical Center, 5000 West National Avenue, Milwaukee, WI, 53295, USA

    Irena Gribovskaja-Rupp, Jung-Myun Kwak, Toku Takahashi & Kirk Ludwig

Authors
  1. Irena Gribovskaja-Rupp
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jung-Myun Kwak
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Toku Takahashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kirk Ludwig
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Toku Takahashi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gribovskaja-Rupp, I., Kwak, JM., Takahashi, T. et al. Nitric oxide regulates polarity of guinea pig distal colon pellet propagation and circular muscle motor response. J Gastroenterol 49, 835–842 (2014). https://doi.org/10.1007/s00535-013-0842-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00535-013-0842-x

Keywords

Search

Navigation